CASE REPORT Open Access

Resection of rectal cancer resemblingsubmucosal tumor that was preoperativelydiagnosed with endoscopic ultrasound-guided biopsyAkimitsu Tanio, Hiroaki Saito* , Keigo Ashida, Shouichi Urushibara, Manabu Yamamoto, Naruo Tokuyasu,Teruhisa Sakamoto, Soichiro Honjo, Yoshihiko Maeta and Yoshiyuki Fujiwara

Abstract

Background: Colorectal cancer (CRC) resembling submucosal tumor (SMT; CRC/SMT) is very rare. Because its biopsyis challenging, accurate preoperative diagnosis is also very rare.

Case presentation: A 55-year-old woman with a high serum carcinoembryonic antigen level underwent a computedtomography colonoscopy, which showed extrinsic rectum compression. A coronal magnetic resonance image showeda 4-cm low-intensity tumor between her rectum and sacrum. Endoscopic ultrasound (EUS) showed a 30-mmlow-echoic lesion originating from the rectum. Pathological examination of specimen obtained with EUS-guided fine-needle aspiration biopsy (EUS-FNAB) revealed adenocarcinoma. Immunohistochemical stainingshowed the tumor to be positive for both CK20 and CDX2 and negative for CK7, indicating that it was arectal cancer. We performed a laparoscopy-assisted low-anterior resection with dissection of the regionallymph nodes after eight chemotherapy cycles. Macroscopically, tumor was completely covered by normalrectal mucosa, but showed a 2-mm bulge on the mucosa. Histological examination revealed a moderately differentiatedadenocarcinoma, mainly located at the subserosal layer and severely invaded to lymphatic and blood vessels. Themucosal layer was not exposed to the cancer components, and her postoperative course was uneventful.

Conclusion: EUS-FNAB was useful in preoperative accurate diagnosis of this very rare tumor. We also review theliterature and discuss CRC/SMT.

Keywords: Colorectal cancer, Endoscopic ultrasound-guided fine needle aspiration biopsy, Submucosal tumor

BackgroundSubmucosal tumor (SMT) usually arises from tissue inthe wall of digestive tract, and its surface is thereforecovered with normal mucosa in most cases. In contrast,gastrointestinal (GI) carcinomas arise from the epithe-lium, and most of their mucosal surfaces typically con-sist of cancerous tissue. SMT-like growth is an unusualpresentation for GI carcinomas, especially in colorectalcancer (CRC). We herein report a rare case of rectalcancer resembling SMT (CRC/SMT) in which endoscopic

ultrasound-guided fine needle aspiration biopsy (EUS-FNAB) was useful in accurate preoperative diagnosis. Wealso review the literature and discuss CRC/SMT.

Case presentationAn asymptomatic 55-year-old woman underwent a de-tailed GI tract examination, as she was found to havehigh serum carcinoembryonic antigen (CEA, 26.6 ng/ml)at a local hospital. She had no event in her past or familyhistory, especially for colorectal neoplasm or other ma-lignancy. Physical examination and blood chemicalexamination were within normal ranges except for highserum CEA level. Computed tomography (CT) colonos-copy revealed extrinsic rectum compression (Fig. 1a). A

* Correspondence: sai10@med.tottori-u.ac.jpDivision of Surgical Oncology, Department of Surgery, School of Medicine,Tottori University Faculty of Medicine, 36-1 Nishi-cho, Yonago 683-8504,Japan

© The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, andreproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link tothe Creative Commons license, and indicate if changes were made.

Tanio et al. Surgical Case Reports (2017) 3:84 DOI 10.1186/s40792-017-0362-7

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coronal magnetic resonance image (MRI) showed a 4-cmlow-intensity tumor between the rectum and sacrum(Fig. 1b); the patient was referred to our hospital forfurther evaluation of this tumor. The 18-FDG positronemission tomography (PET) and CT scans indicated high18-FDG uptake in the primary tumor (SUVmax: 3.34;Fig. 2a), with enlarged para-aortic lymph node (SUVmax:2.58; Fig. 2b) and anterosuperior segment of right hepaticlobe (SUVmax: 2.74; Fig. 2c). Colonoscopy showed extrin-sic rectum compression, but no change in her rectal mu-cosa (Fig. 3a). Pathological examination of rectum biopsyspecimen showed normal rectal mucosa. Endoscopicultrasound (EUS) showed a 30-mm, low-echoic lesionoriginating from the rectum (Fig. 3b). Pathological exam-ination of biopsied specimen obtained with EUS-guidedfine-needle aspiration biopsy (EUS-FNAB) revealedadenocarcinoma. Immunohistochemical staining showedthat the specimen was positive for both cytokeratin 20

(CK20; Fig. 3c) and caudal-type homeobox 2 (CDX2;Fig. 3d) and negative for cytokeratin-7 (CK7), which indi-cated that it had originated from rectal cancer. Weplanned to perform low-anterior resection with dissectionof the regional lymph nodes and an enlarged para-aorticlymph node under the diagnosis of rectal cancer and pos-sible metastasis to liver and para-aortic lymph node,followed by resection of possible liver metastasis afterpostoperative chemotherapy. Because of a possibilitythat tumor had invaded to the sacrum, however, weperformed neoadjuvant chemotherapy with capecita-bine and oxaliplatin. The tumor shrank by 38% after8 courses of chemotherapy, and we performed alaparoscopy-assisted low-anterior resection with dis-section of the regional lymph nodes as planned. Al-though we confirmed direct invasion of the tumor tohypogastric nerve during the surgery, the tumor didnot invade to the sacrum. An enlarged para-aortic lymph

a b

Fig. 1 a CT colonoscopy revealed extrinsic compression of rectum. b Coronal magnetic resonance imaging (MRI) showed 4-cm low-intensitytumor between rectum and sacrum

a b

c

Fig. 2 The 8-FDG positron emission tomography (PET) and CT scans indicate high 18-FDG uptake in (a) the primary tumor (SUVmax: 3.34);(b) enlarged para-aortic lymph node (SUVmax: 2.58); and (c) anterosuperior segment of right hepatic lobe (SUVmax: 2.74)

Tanio et al. Surgical Case Reports (2017) 3:84 Page 2 of 5

node was also removed. Macroscopically, the tumor wascompletely covered by normal rectal mucosa (Fig. 4a), al-though there was a 2-mm bulge of elevated lesion on themucosa (Fig. 4b). Histologically, the tumor was composedfrom moderately differentiated adenocarcinoma (Fig. 5a)and was mainly located at subserosal region with severe in-vasion to lymphatic and blood vessels (Fig. 5b). However,the mucosal surface showed no exposure of the cancercomponent (Fig. 5c). Metastases were found in two lymphnodes of mesorectum (#251) and in one lymph node alongthe superior rectal artery (#252), although there was nometastasis in the para-aortic lymph node dissected. Thepostoperative course was uneventful. The patient is cur-rently undergoing chemotherapy for liver metastasis in theoutpatient clinic of our hospital.

DiscussionCarcinomas of the digestive tract arise from the mucosalepithelium; most of their mucosal surfaces consist ofcancerous tissues. Although cancer cells then infiltrateboth horizontally and vertically, the dominant directiondepends on the nature of the cancer cells. Some intes-tinal cancers dominantly infiltrate in a vertical directionwithout massive invasion along the horizontal plane. Asa result, the internal intestinal surfaces over these tu-mors are mostly covered with normal mucosa, andtherefore manifest as SMTs. This type of tumor is some-times called a carcinoma resembling an SMT; and al-though it is extremely rare, has been reported in theesophagus [1], stomach [2], and colon and rectum [3, 4].A report that reviewed 70 reported cases of CRC/SMT

a b

c d

Fig. 3 a Colonoscopy also showed extrinsic compression of rectum, but no change in rectal mucosa. b Endoscopic ultrasound (EUS) showed a30-mm low echoic lesion originating from rectum. Immunohistochemical staining of biopsy specimen obtained by EUS-FNAB showed that tumorwas positive for both (c) CK20 and (d) CDX2

a b

Fig. 4 a Macroscopically, the tumor was completely covered by normal rectal mucosa. b The formalin-fixed resected specimen showed a 2-mmbulge above the mucosa level

Tanio et al. Surgical Case Reports (2017) 3:84 Page 3 of 5

found it to be characterized by small tumor size, highrates of poorly differentiated adenocarcinoma or mucin-ous adenocarcinoma, and invasiveness (including highrates of lymph node metastasis and lymphatic vessel in-vasion) [4].Two points make our case different from previously

reported CRC/SMT. Firstly, the tumor was completelycovered by normal rectal mucosa in our case. Most tu-mors reported previously showed at least faint mucosalchanges, such as erosion and ulceration, which aremicroscopically consistent with exposure of carcinomacells. Because most of the cancer on our case was lo-cated subserosally with no exposure of cancer cells onmucosal surface, metastatic rectal cancer was consid-ered. In this regard, immunohistochemical staining ofthe biopsied specimen showed the tumor was positivefor CK20 and negative for CK7, indicating the strong

possibility that our patient had primary rectal cancer. Tothe best of our knowledge, only four cases (including thepresent case) have been reported of CRC/SMT that werecompletely covered with normal rectal mucosa (Table 1)[5–7]. Why no cancer cells were exposed on the mucosallayer remains unclear. Cancer may arise from ectopicmucosal cells in the rectal wall. Further investigationsare required to show the detailed mechanism.Secondly, our case clearly showed that EUS-FNAB is

useful for accurate preoperative diagnosis of CRC/SMT.EUS-FNAB was recently shown to be useful in accuratepreoperative diagnosis of gastrointestinal stromal tumor(GIST) [8] and pancreatic cancer [9]. Previous reportshave shown the difficulty of preoperative CRC/SMTdiagnosis, because of the difficulty of obtaining biopsyspecimens. Therefore, EUS-FNAB should be consideredto make accurate preoperative SMT diagnoses in colon

Fig. 5 a Histologically, the tumor was composed of moderately differentiated adenocarcinoma. b The carcinoma was mainly located at subserosaand had severely invaded to lymphatic and blood vessels. c Adenocarcinoma was observed in the submucosal layer and the mucosal surfaceshowed no exposure of the cancer component

Table 1 Reported cases of colorectal cancer resembling SMT in which tumor was completely covered with normal colorectal mucosa

Case Year Age(years)

Gender Locationa Size(cm)

Endoscopicfindings

Depth ofinvasionb

Histologicdiagnosis ofbiopsy specimen

Histologicdiagnosis ofresected specimenc

Lymphnodemetastasis

Distantmetastasis

Reference

1 2005 57 M Rb 10 None A Unknown Muc Absent Unknown 5

2 2011 82 M S 8 None SS Normal mucosa Muc Absent Absent 6

3 2014 79 M Ra 2.6 Erosion SE Not performed Mod Absent Absent 7

4 2017 55 F RS 4 None SS Normal mucosa Mod Present Livermetastasis

Our case

aLocation. Ra upper rectum, Rb lower rectum, RS rectosigmoid, S sigmoid colonbDepth of invasion. A adventitia, SE serosa, SS subserosacHistologic diagnosis of resected specimen. Mod moderately differentiated adenocarcinoma, Muc mucinous carcinoma

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and rectum. To our knowledge, our case is the first touse EUS-FNAB for an accurate preoperative diagnosis ofCRC/SMT.

ConclusionWe should keep in mind that colorectal cancer canpresent with SMT-like growth. Furthermore, EUS-FNABis useful for preoperative accurate diagnosis of this rarecolorectal cancer.

Received: 3 April 2017 Accepted: 11 July 2017

Authors’ contributionsAT contributed to the drafting of the manuscript. KA, SU, MY, NT, TS, SH, andYM contributed to the critical revision of the manuscript. HS and YFcontributed to the final approval of the manuscript. All authors read andapproved the final manuscript.

Consent for publicationConsent for publication was obtained from the patients.

Competing interestsThe authors declare that they have no competing interests.

Publisher’s NoteSpringer Nature remains neutral with regard to jurisdictional claims in publishedmaps and institutional affiliations.

Received: 3 April 2017 Accepted: 11 July 2017

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AbstractBackgroundCase presentationConclusion

BackgroundCase presentationDiscussionConclusionReferences